Role of chaperone-mediated autophagy in metabolism

FEBS Journal

Volumn , Issue , 2016, Pages 2403-2413

  Tasset, Inmaculada ^a   Cuervo, Ana Maria ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

chaperones; diabetes; fatty liver; glucose metabolism; lipid metabolism; lysosomes; proteases; proteolysis

Indexed keywords

AGING; CANCER CELL; CELL ENERGY; CELL METABOLISM; CELL STRESS; CHAPERONE-MEDIATED AUTOPHAGY; GLUCOSE METABOLISM; HUMAN; LIPID METABOLISM; LYSOSOME; METABOLIC DISORDER; NONHUMAN; NUTRITION; PATHOGENESIS; PRIORITY JOURNAL; PROTEOMICS; REVIEW; UPREGULATION;

EID: 84978144234     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13677     Document Type: Review

References (61)

1. Zhang H & Baehrecke EH (2015) Eaten alive: novel insights into autophagy from multicellular model systems. Trends Cell Biol 25, 376–387.
2. Fernandez AF & Lopez-Otin C (2015) The functional and pathologic relevance of autophagy proteases. J Clin Invest 125, 33–41.
3. Mizushima N, Levine B, Cuervo AM & Klionsky DJ (2008) Autophagy fights disease through cellular self-digestion. Nature 451, 1069–1075.
4. Sahu R, Kaushik S, Clement CC, Cannizzo ES, Scharf B, Follenzi A, Potolicchio I, Nieves E, Cuervo AM & Santambrogio L (2011) Microautophagy of cytosolic proteins by late endosomes. Dev Cell 20, 131–139.
5. Dubouloz F, Deloche O, Wanke V, Cameroni E & De Virgilio C (2005) The TOR and EGO protein complexes orchestrate microautophagy in yeast. Mol Cell 19, 15–26.
6. Cuervo AM & Wong E (2014) Chaperone-mediated autophagy: roles in disease and aging. Cell Res 24, 92–104.
7. Kaushik S & Cuervo AM (2012) Chaperone-mediated autophagy: a unique way to enter the lysosome world. Trends Cell Biol 22, 407–417.
8. Arias E & Cuervo AM (2011) Chaperone-mediated autophagy in protein quality control. Curr Opin Cell Biol 23, 184–189.
9. Valdor R, Mocholi E, Botbol Y, Guerrero-Ros I, Chandra D, Koga H, Gravekamp C, Cuervo AM & Macian F (2014) Chaperone-mediated autophagy regulates T cell responses through targeted degradation of negative regulators of T cell activation. Nat Immunol 15, 1046–1054.
10. Yang Q, She H, Gearing M, Colla E, Lee M, Shacka JJ & Mao Z (2009) Regulation of neuronal survival factor MEF2D by chaperone-mediated autophagy. Science 323, 124–127.
11. Xie W, Zhang L, Jiao H, Guan L, Zha J, Li X, Wu M, Wang Z, Han J & You H (2015) Chaperone-mediated autophagy prevents apoptosis by degrading BBC3/PUMA. Autophagy 11, 1623–1635.
12. Hubbi ME, Hu H, Kshitiz Ahmed I, Levchenko A & Semenza GL (2013) Chaperone-mediated autophagy targets hypoxia-inducible factor-1alpha (HIF-1alpha) for lysosomal degradation. J Biol Chem 288, 10703–10714.
13. Ferreira JV, Fofo H, Bejarano E, Bento CF, Ramalho JS, Girao H & Pereira P (2013) STUB1/CHIP is required for HIF1A degradation by chaperone-mediated autophagy. Autophagy 9, 1349–1366.
14. Park C, Suh Y & Cuervo AM (2015) Regulated degradation of Chk1 by chaperone-mediated autophagy in response to DNA damage. Nat Commun 6, 6823.
15. Lv L, Li D, Zhao D, Lin R, Chu Y, Zhang H, Zha Z, Liu Y, Li Z, Xu Y et al. (2011) Acetylation targets the M2 isoform of pyruvate kinase for degradation through chaperone-mediated autophagy and promotes tumor growth. Mol Cell 42, 719–730.
16. Schneider JL, Suh Y & Cuervo AM (2014) Deficient chaperone-mediated autophagy in liver leads to metabolic dysregulation. Cell Metab 20, 417–432.
17. Xia HG, Najafov A, Geng J, Galan-Acosta L, Han X, Guo Y, Shan B, Zhang Y, Norberg E, Zhang T et al. (2015) Degradation of HK2 by chaperone-mediated autophagy promotes metabolic catastrophe and cell death. J Cell Biol 210, 705–716.
18. Kaushik S & Cuervo AM (2015) Degradation of lipid droplet-associated proteins by chaperone-mediated autophagy facilitates lipolysis. Nat Cell Biol 17, 759–770.
19. Dice JF (1990) Peptide sequences that target cytosolic proteins for lysosomal proteolysis. Trends Biochem Sci 15, 305–309.
20. Chiang H, Terlecky S, Plant C & Dice JF (1989) A role for a 70-kilodalton heat shock protein in lysosomal degradation of intracellular proteins. Science 246, 382–385.
21. Cuervo AM & Dice JF (1996) A receptor for the selective uptake and degradation of proteins by lysosomes. Science 273, 501–503.
22. Bandyopadhyay U, Kaushik S, Varticovski L & Cuervo AM (2008) The chaperone-mediated autophagy receptor organizes in dynamic protein complexes at the lysosomal membrane. Mol Cell Biol 28, 5747–5763.
23. Rout AK, Strub MP, Piszczek G & Tjandra N (2014) Structure of transmembrane domain of lysosome-associated membrane protein type 2a (LAMP-2A) reveals key features for substrate specificity in chaperone-mediated autophagy. J Biol Chem 289, 35111–35123.
24. Salvador N, Aguado C, Horst M & Knecht E (2000) Import of a cytosolic protein into lysosomes by chaperone-mediated autophagy depends on its folding state. J Biol Chem 275, 27447–27456.
25. Agarraberes F & Dice JF (2001) A molecular chaperone complex at the lysosomal membrane is required for protein translocation. J Cell Sci 114, 2491–2499.
26. Cuervo AM, Dice JF & Knecht E (1997) A population of rat liver lysosomes responsible for the selective uptake and degradation of cytosolic proteins. J Biol Chem 272, 5606–5615.
27. Bandyopadhyay U, Sridhar S, Kaushik S, Kiffin R & Cuervo AM (2010) Identification of regulators of chaperone-mediated autophagy. Mol Cell 39, 535–547.
28. Cuervo AM & Dice JF (2000) Regulation of lamp2a levels in the lysosomal membrane. Traffic 1, 570–583.
29. Kiffin R, Christian C, Knecht E & Cuervo AM (2004) Activation of chaperone-mediated autophagy during oxidative stress. Mol Biol Cell 15, 4829–4840.
30. Cuervo AM, Knecht E, Terlecky SR & Dice JF (1995) Activation of a selective pathway of lysosomal proteolysis in rat liver by prolonged starvation. Am J Physiol 269, C1200–C1208.
31. Anguiano J, Garner TP, Mahalingam M, Das BC, Gavathiotis E & Cuervo AM (2013) Chemical modulation of chaperone-mediated autophagy by retinoic acid derivatives. Nat Chem Biol 9, 374–382.
32. Arias E, Koga H, Diaz A, Mocholi E, Patel B & Cuervo AM (2015) Lysosomal mTORC2/PHLPP1/Akt regulate chaperone-mediated autophagy. Mol Cell 59, 270–284.
33. Massey AC, Kaushik S, Sovak G, Kiffin R & Cuervo AM (2006) Consequences of the selective blockage of chaperone-mediated autophagy. Proc Nat Acad Sci USA 103, 5905–5910.
34. Schneider JL, Villarroya J, Diaz-Carretero A, Patel B, Urbanska AM, Thi MM, Villarroya F, Santambrogio L & Cuervo AM (2015) Loss of hepatic chaperone-mediated autophagy accelerates proteostasis failure in aging. Aging Cell 14, 249–264.
35. Kaushik S, Massey A, Mizushima N & Cuervo AM (2008) Constitutive activation of chaperone-mediated autophagy in cells with impaired macroautophagy. Mol Biol Cell 19, 2179–2192.
36. Koga H, Martinez-Vicente M, Macian F, Verkhusha VV & Cuervo AM (2011) A photoconvertible fluorescent reporter to track chaperone-mediated autophagy. Nat Commun 2, 386.
37. Backer JM, Bourret L & Dice JF (1983) Regulation of catabolism of microinjected ribonuclease A requires the amino-terminal 20 amino acids. Proc Natl Acad Sci USA 80, 2166–2170.
38. Berger JJ & Dice JF (1985) Effect of serum deprivation and replacement on proteolysis in cultured human fibroblasts. Prog Clin Biol Res 180, 479–481.
39. Wing SS, Chiang HL, Goldberg AL & Dice JF (1991) Proteins containing peptide sequences related to KFERQ are selectively depleted in liver and heart, but not skeletal muscle, of fasted rats. Biochem J 275, 165–169.
40. Abeliovich H, Dunn WA Jr, Kim J & Klionsky DJ (2000) Dissection of autophagosome biogenesis into distinct nucleation and expansion steps. J Cell Biol 151, 1025–1034.
41. Mizushima N, Yamamoto A, Matsui M, Yoshimori T & Ohsumi Y (2004) In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 15, 1101–1111.
42. Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, Komatsu M, Tanaka K, Cuervo AM & Czaja MJ (2009) Autophagy regulates lipid metabolism. Nature 458, 1131–1135.
43. Kon M, Kiffin R, Koga H, Chapochnick J, Macian F, Varticovski L & Cuervo AM (2011) Chaperone-mediated autophagy is required for tumor growth. Sci Transl Med 3, 109ra117.
44. Zhang C & Cuervo AM (2008) Restoration of chaperone-mediated autophagy in aging liver improves cellular maintenance and hepatic function. Nat Med 14, 959–965.
45. Cuervo AM, Terlecky SR, Dice JF & Knecht E (1994) Selective binding and uptake of ribonuclease A and glyceraldehyde-3-phosphate dehydrogenase by isolated rat liver lysosomes. J Biol Chem 269, 26374–26380.
46. Lu W, Zhang Y, McDonald DO, Jing H, Carroll B, Robertson N, Zhang Q, Griffin H, Sanderson S, Lakey JH et al. (2014) Dual proteolytic pathways govern glycolysis and immune competence. Cell 159, 1578–1590.
47. Chweiger M & Zechner R (2015) Breaking the barrier–chaperone-mediated autophagy of perilipins regulates the lipolytic degradation of fat. Cell Metab 22, 60–61.
48. Kaushik S & Cuervo AM (2016) AMPK-dependent phosphorylation of lipid droplet protein PLIN2 triggers its degradation by CMA. Autophagy 12, 439–447.
49. Cuervo AM & Dice JF (2000) Age-related decline in chaperone-mediated autophagy. J Biol Chem 275, 31505–31513.
50. Kiffin R, Kaushik S, Zeng M, Bandyopadhyay U, Zhang C, Massey AC, Martinez-Vicente M & Cuervo AM (2007) Altered dynamics of the lysosomal receptor for chaperone-mediated autophagy with age. J Cell Sci 120, 782–791.
51. Rodriguez-Navarro JA, Kaushik S, Koga H, Dall'armi C, Shui G, Wenk MR, Di Paolo G & Cuervo AM (2012) Inhibitory effect of dietary lipids on chaperone-mediated autophagy. Proc Natl Acad Sci USA 109, E705–E714.
52. Das S, Seth RK, Kumar A, Kadiiska MB, Michelotti G, Diehl AM & Chatterjee S (2013) Purinergic receptor X7 is a key modulator of metabolic oxidative stress-mediated autophagy and inflammation in experimental nonalcoholic steatohepatitis. Am J Physiol Gastrointest Liver Physiol 305, G950–G963.
53. Kaushik S, Massey AC & Cuervo AM (2006) Lysosome membrane lipid microdomains: novel regulators of chaperone-mediated autophagy. EMBO J 25, 3921–3933.
54. Sooparb S, Price SR, Shaoguang J & Franch HA (2004) Suppression of chaperone-mediated autophagy in the renal cortex during acute diabetes mellitus. Kidney Int 65, 2135–2144.
55. Franch H, Sooparb S, Du J & Brown N (2001) A mechanism regulating proteolysis of specific proteins during renal tubular cell growth. J Biol Chem 276, 19126–19131.
56. Napolitano G, Johnson JL, He J, Rocca CJ, Monfregola J, Pestonjamasp K, Cherqui S & Catz SD (2015) Impairment of chaperone-mediated autophagy leads to selective lysosomal degradation defects in the lysosomal storage disease cystinosis. EMBO Mol Med 7, 158–174.
57. Saha T (2012) LAMP2A overexpression in breast tumors promotes cancer cell survival via chaperone-mediated autophagy. Autophagy 8, 1643–1656.
58. Li L, Fang R, Liu B, Shi H, Wang Y, Zhang W, Zhang X & Ye L (2015) Deacetylation of tumor-suppressor MST1 in Hippo pathway induces its degradation through HBXIP-elevated HDAC6 in promotion of breast cancer growth. Oncogene doi:10.1038/onc.2015.476. [Epub ahead of print]
59. Kubota C, Torii S, Hou N, Saito N, Yoshimoto Y, Imai H & Takeuchi T (2010) Constitutive reactive oxygen species generation from autophagosome/lysosome in neuronal oxidative toxicity. J Biol Chem 285, 667–674.
60. Quintavalle C, Di Costanzo S, Zanca C, Tasset I, Fraldi A, Incoronato M, Mirabelli P, Monti M, Ballabio A, Pucci P et al. (2014) Phosphorylation-regulated degradation of the tumor-suppressor form of PED by chaperone-mediated autophagy in lung cancer cells. J Cell Physiol 229, 1359–1368.
61. Vakifahmetoglu-Norberg H, Kim M, Xia HG, Iwanicki MP, Ofengeim D, Coloff JL, Pan L, Ince TA, Kroemer G, Brugge JS et al. (2013) Chaperone-mediated autophagy degrades mutant p53. Genes Dev 27, 1718–1730.